University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 8-1-1999 Systematics of the Eucestoda: Advances Toward a New Phylogenetic Paradigm and Observations on the Early Diversification of apewormsT and Vertebrates Eric P. Hoberg United States Department of Agriculture, Agricultural Research Service, [email protected] Scott Lyell Gardner University of Nebraska - Lincoln, [email protected] Ronald A. Campbell University of Massachusetts - Dartmouth, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs Part of the Biodiversity Commons, Evolution Commons, and the Parasitology Commons Hoberg, Eric P.; Gardner, Scott Lyell; and Campbell, Ronald A., "Systematics of the Eucestoda: Advances Toward a New Phylogenetic Paradigm and Observations on the Early Diversification of apewormsT and Vertebrates" (1999). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 56. https://digitalcommons.unl.edu/parasitologyfacpubs/56 This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Systematic Parasitology (1999) 42: 1–12. Copyright 1999, Kluwer Academic Publishers. Used by permission. Systematics of the Eucestoda: Advances Toward a New Phylogenetic Paradigm, and Observations on the Early Diversification of Tapeworms and Vertebrates* Eric P. Hoberg1, Scott L. Gardner2 & Ronald A. Campbell3 1Biosystematics and National Parasite Collection Unit, United States Department of Agriculture, Agricultural Research Service, BARC East No. 1180, 10300 Baltimore Avenue, Beltsville, Maryland 20715, USA ([email protected]) 2Harold W. Manter Laboratory of Parasitology, W-529 Nebraska Hall, University of Nebraska, Lincoln, Neb. 68588-0514, USA 3Department of Biology, University of Massachusetts-Dartmouth, N. Dartmouth, Massachusetts 02747, USA Accepted for publication July 9, 1998. Abstract Evolutionary relationships of the Eucestoda have received intense but sporadic attention over the past century. Since 1996, the landscape has dramatically changed with respect to our knowledge of the phy- logenetic relationships among the tapeworms. The 2nd International Workshop for Tapeworm System- atics (IWTS) held in Lincoln, Nebraska in October of that year provided the catalyst for development of novel hypotheses for inter-and intra-ordinal phylogeny. The working-group structure of the 2nd IWTS and results of phylogenetic studies are briefly introduced in the present manuscript. Higher-level phylog- enies derived from parsimony analysis of independent data bases representing comparative morphology or molecular sequences were largely congruent and supported monophyly for the Eucestoda. The Caryo- phyllidea are basal; difossate forms such as the Pseudophyllidea are primitive; tetrafossates including the Tetraphyllidea, Proteocephalidea, Nippotaeniidea, Tetrabothriidea and Cyclophyllidea are derived; and hypotheses differed in the placement of the Trypanorhyncha and the Diphyllidea. These studies may pro- vide a foundation for resolution of inter-and intra-ordinal relationships for the tapeworms. Additionally, the first comprehensive phylogenetic hypotheses for the Pseudophyllidea, Diphyllidea, Trypanorhyncha, the paraphyletic Tetraphyllidea + Lecanicephalidea, Proteocephalidea and Cyclophyllidea were developed during and subsequent to the 2nd IWTS. The stage is now set for continued and rapid advances in our understanding of the eucestodes. These studies have also served to re-emphasise the rich genealogical di- versity of tapeworms and the temporally deep history for their origin. A co-evolutionary history and ra- diation of eucestodes may involve deep co-speciation with vertebrate host taxa, accompanied by some level of colonisation and extinction, extending into the Palaeozoic, minimally 350-420 million years ago. Introduction issues related to the Eucestoda Southwell, 1930 has dramatically increased since the late 1980s Interest in the systematics of the tapeworms has es- (see Brooks & McLennan, 1993; Hoberg et al., 1997b; calated over the past decade. The first phylogenetic Hoberg, 1997; Mariaux, 1998). Higher-level relation- study of cestodes, a treatment of the Proteocepha- ships among the orders have been examined only re- lidea Mola, 1928 was published by Brooks (1978) cently for the first time (e.g. Brookset al., 1991; Brooks more than 20 years ago, but the number of papers & McLennan, 1993), whereas most previous studies addressing phylogeny, co-evolution and historical focused on species or generic genealogical diversity. Interest in the systematics and taxonomy of * A report of results of phylogenetic analyses conducted during tapeworms led to the 1st International Work- the 2nd International Workshop for Tapeworm Systematics, Lin- shop for Tapeworm Systematics (IWTS) chaired coln, Nebraska, October 2-6, 1996; E.P. Hoberg, S.L. Gardner and R.A. Campbell, organizers. Contributions edited by E.P. Hoberg. 1 2 S Y S TEMATIC PARA S ITOLOGY (1999), 42: 1-12. by Claude Vaucher and Jean Mariaux in Ge- of order (chair: E.P. Hoberg); (2) molecular sys- neva, Switzerland in 1993 (Mariaux & Vaucher, tematics (J. Mariaux); (3) ultrastructural characters 1994). At this seminal meeting the conceptual of spermatozoa and spermiogenesis (J.-L. Justine); roots were created to build a broad and coopera- (4) Pseudophyllidea Carus, 1863 (R.A. Bray); (5) tive international research program addressing Tetraphyllidea Carus, 1863, Trypanorhyncha Dies- significant questions in eucestode systematics. ing, 1863 and associated orders (R.A. Campbell); Evolutionary relationships of the eucestodes have (6) Proteocephalidea (A. Rego); and (7) Cyclophyl- received intense but sporadic attention over the past lidea van Beneden in Braun, 1900 (A. Jones). Ad- century, but there has never been a general consen- ditional groups focused on relationships of genera sus among the various hypotheses (see Brooks et al., within families (e.g. Hymenolepididae Ariola, 1899, 1991; Mariaux, 1996; Hoberg et al., 1997b). Conflict- Anoplocephalidae Cholodkowsky, 1902, Metadile- ing opinions over the adequacy of different classes pididae Spasskii, 1959, Paruterinidae Fuhrmann, of morphological and molecular characters as in- 1907) and species within genera (e.g. Taeniidae dicators of relationship, the application of differ- Ludwig, 1886 and species of Taenia Linnaeus, 1758). ent methodologies for phylogenetic reconstruction, Each Working Team produced a summary of and untested assumptions of host-parasite co-spe- characters representing putative homologies for ciation (e.g. the concept that the phylogeny of hosts morphological attributes (including those from mirrors that of the parasite taxon) have contributed light and electron microscopy), ontogeny, or mo- to the current situation (Mariaux, 1996). Although lecular sequence data. Putative transformation se- the most recent diagnostic keys provided compre- ries generated from character descriptions were hensive coverage to the generic level, there was no polarised relative to taxonomic outgroup(s) (Mad- general attempt to reflect evolutionary relation- dison et al., 1984) and summarised in numerical ships (Khalil et al., 1994). Assessments of phyloge- character matrices. These constituted the basis netic diversity, however, have become increasingly for development of phylogenetic hypotheses for important with the advent of biodiversity surveys each taxon under study. Parsimony analyses were and inventories in conservation biology, analyses of conducted with PAUP 3.1.1 and MacClade 3.05 host-parasite co-speciation and historical biogeog- (Swofford, 1993; Maddison & Maddison, 1992). raphy, and strategic research involving agricultur- Phylogenetic hypotheses resulting from these ally and medically important taxa (Hoberg, 1997). analyses represented the first concerted effort to These issues formed the foundation for the 2nd develop a comprehensive knowledge of relation- IWTS held in Lincoln, Nebraska in 1996 (Hoberg et ships for the Eucestoda. In this context, hierarchical al., 1997a). The Workshop was convened to explore and top-down analyses initially addressed higher new and concrete ideas for future progress in tape- level relationships and were in many cases used worm systematics and to work toward standardis- to identify outgroups for sequential and more in- ing research programmes at the international level clusive levels of study within orders. In contrast, with emphasis on phylogenetic systematic analy- bottom-up analyses focused on lower taxonomic sis (Hennig, 1966; Wiley 1981; Wiley et al., 1991). levels and sampled representative genera and spe- Results of the Workshop are now summarised in cies to estimate phylogenetic structure within and part and presented herein as a series of papers ad- among ordinal-level groups. Thus, an array of dressing various aspects of eucestode phylogeny. characters with different levels of universality (see Wiley, 1981) appropriate to these philosophically Methods and rationale disparate but complementary approaches were used in the elucidation of phylogeny. A subsequent The structure and rationale for